Light, heat, action: Neural control of fruit fly behaviour

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1677, 2015, Pages

  Owald, David ^a   Lin, Suewei ^a   Waddell, Scott ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Behaviour; Cellular resolution; Drosophila; Optogenetics; Reporters; Thermogenetics

Indexed keywords

BEHAVIOR; CELLS AND CELL COMPONENTS; FLY; GENETIC ENGINEERING; LIGHT EFFECT; NERVOUS SYSTEM; NEUROLOGY;

ANIMALIA; DROSOPHILA MELANOGASTER;

ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; BIOLOGICAL MODEL; DROSOPHILA MELANOGASTER; GENE; GENE EXPRESSION; GENETICS; HEAT; LEARNING; LIGHT; MEMORY; NERVE CELL; NERVE TRACT; OPTOGENETICS; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENES, INSECT; HOT TEMPERATURE; LEARNING; LIGHT; MEMORY; MODELS, ANIMAL; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NEURONS; OPTOGENETICS;

EID: 84938535000     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0211     Document Type: Review

References (178)

1. Takemura SY et al. 2013 A visual motion detection circuit suggested by Drosophila connectomics. Nature 500, 175–181. (doi:10.1038/nature12450)
2. Kleinfeld D et al. 2011 Large-scale automated histology in the pursuit of connectomes. J. Neurosci. 31, 16 125–16 138. (doi:10.1523/JNEUROSCI.4077-11.2011)
3. Toga AW, Clark KA, Thompson PM, Shattuck DW, Van Horn JD. 2012 Mapping the human connectome. Neurosurgery 71, 1–5. doi:10.1227/NEU.0b013e318258e9ff
4. Kuan L et al. 2015 Neuroinformatics of the Allen Mouse Brain Connectivity Atlas. Methods 73, 4–17. (doi:10.1016/j.ymeth.2014.12.013)
5. White JG, Southgate E, Thomson JN, Brenner S. 1986 The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1–340. (doi:10.1098/rstb.1986.0056)
6. Varshney LR, Chen BL, Paniagua E, Hall DH, Chklovskii DB. 2011 Structural properties of the Caenorhabditis elegans neuronal network. PLoS Comput. Biol. 7, e1001066. (doi:10.1371/journal.pcbi.1001066)
7. Bargmann CI, Marder E. 2013 From the connectome to brain function. Nat. Methods 10, 483–490. (doi:10.1038/nmeth.2451)
8. Weiner J. 2014 Time, love, memory: a great biologist and his quest for the origins of behavior. New York, NY: Vintage Books.
9. Lewis EB. 1978 A gene complex controlling segmentation in Drosophila. Nature 276, 565–570. (doi:10.1038/276565a0)
10. Nusslein-Volhard C, Wieschaus E. 1980 Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801. (doi:10.1038/287795a0)
11. Konopka RJ, Benzer S. 1971 Clock mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 68, 2112–2116. (doi:10.1073/pnas.68.9.2112)
12. Hotta Y, Benzer S. 1976 Courtship in Drosophila mosaics: sex-specific foci for sequential action patterns. Proc. Natl Acad. Sci. USA 73, 4154–4158. (doi:10.1073/pnas.73.11.4154)
13. Quinn WG, Harris WA, Benzer S. 1974 Conditioned behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 71, 708–712. (doi:10.1073/pnas.71.3.708)
14. Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, Brummel T, Benzer S. 2007 Prandiology of Drosophila and the CAFE assay. Proc. Natl Acad. Sci. USA 104, 8253–8256. (doi:10.1073/pnas.0702726104)
15. Al-Anzi B, Sapin V, Waters C, Zinn K, Wyman RJ, Benzer S. 2009 Obesity-blocking neurons in Drosophila. Neuron 63, 329–341. (doi:10.1016/j.neuron.2009.07.021)
16. Al-Anzi B, Armand E, Nagamei P, Olszewski M, Sapin V, Waters C, Zinn K, Wyman RJ, Benzer S. 2010 The leucokinin pathway and its neurons regulate meal size in Drosophila. Curr. Biol. 20, 969–978. (doi:10.1016/j.cub.2010.04.039)
17. Chen S, Lee AY, Bowens NM, Huber R, Kravitz EA. 2002 Fighting fruit flies: a model system for the study of aggression. Proc. Natl Acad. Sci. USA 99, 5664–5668. (doi:10.1073/pnas.082102599)
18. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G. 2000 Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834–1837. (doi:10.1126/science.287.5459.1834)
19. Hendricks JC et al. 2000 Rest in Drosophila is a sleep-like state. Neuron 25, 129–138. (doi:10.1016/S0896-6273(00)80877-6)
20. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S. 2009 A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139, 416–427. (doi:10.1016/j.cell.2009.08.035)
21. Lin S, Owald D, Chandra V, Talbot C, Huetteroth W, Waddell S. 2014 Neural correlates of water reward in thirsty Drosophila. Nat. Neurosci. 17, 1536–1542. (doi:10.1038/nn.3827)
22. Lin YJ, Seroude L, Benzer S. 1998 Extended lifespan and stress resistance in the Drosophila mutant methuselah. Science 282, 943–946. (doi:10.1126/science.282.5390.943)
23. Buchanan RL, Benzer S. 1993 Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron 10, 839–850. (doi:10.1016/0896-6273(93)90200-B)
24. Min KT, Benzer S. 1997 Spongecake and eggroll: two hereditary diseases in Drosophila resemble patterns of human brain degeneration. Curr. Biol. 7, 885–888. (doi:10.1016/S0960-9822(06)00378-2)
25. Kretzschmar D, Hasan G, Sharma S, Heisenberg M, Benzer S. 1997 The swiss cheese mutant causes glial hyperwrapping and brain degeneration in Drosophila. J. Neurosci. 17, 7425–7432.
26. Lai SL, Lee T. 2006 Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9, 703–709. (doi:10.1038/nn1681)
27. Riabinina O et al. 2015 Improved and expanded Q-system reagents for genetic manipulations. Nat. Methods 12, 219–222. (doi:10.1038/nmeth.3250)
28. O’Kane CJ, Gehring WJ. 1987 Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl Acad. Sci. USA 84, 9123–9127. (doi:10.1073/pnas.84.24.9123)
29. Kaiser K. 1993 Second generation enhancer traps. Curr. Biol. 3, 560–562. (doi:10.1016/0960-9822(93)90058-V)
30. Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K. 1995 Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15, 45–54. (doi:10.1016/0896-6273(95)90063-2)
31. Rubin GM, Spradling AC. 1982 Genetic transformation of Drosophila with transposable element vectors. Science 218, 348–353. (doi:10.1126/science.6289436)
32. Rubin GM, Spradling AC. 1983 Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 11, 6341–6351. (doi:10.1093/nar/11.18.6341)
33. Brand AH, Perrimon N. 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415.
34. Fisher F, Jayaraman PS, Goding CR. 1991 C-myc and the yeast transcription factor PHO4 share a common CACGTG-binding motif. Oncogene 6, 1099–1104.
35. Budnik V, White K. 1987 Genetic dissection of dopamine and serotonin synthesis in the nervous system of Drosophila melanogaster. J. Neurogenet. 4, 309–314. (doi:10.3109/01677068709102351)
36. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, Birman S. 2003 Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54, 618–627. (doi:10.1002/neu.10185)
37. Liu C et al. 2012 A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488, 512–516. (doi:10.1038/nature11304)
38. Burke CJ et al. 2012 Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492, 433–437. (doi:10.1038/nature11614)
39. Kitamoto T, Ikeda K, Salvaterra PM. 1995 Regulation of choline acetyltransferase/lacZ fusion gene expression in putative cholinergic neurons of Drosophila melanogaster. J. Neurobiol. 28, 70–81. (doi:10.1002/neu.480280107)
40. Lebestky T et al. 2009 Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64, 522–536. (doi:10.1016/j.neuron.2009.09.031)
41. Ueno T, Tomita J, Tanimoto H, Endo K, Ito K, Kume S, Kume K. 2012 Identification of a dopamine pathway that regulates sleep and arousal in Drosophila. Nat. Neurosci. 15, 1516–1523. (doi:10.1038/nn.3238)
42. Liu Q, Liu S, Kodama L, Driscoll MR, Wu MN. 2012 Two dopaminergic neurons signal to the dorsal fanshaped body to promote wakefulness in Drosophila. Curr. Biol. 22, 2114–2123. (doi:10.1016/j.cub.2012.09.008)
43. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, Hirsh J, Miesenböck G. 2009 Writing memories with light-addressable reinforcement circuitry. Cell 139, 405–415. (doi:10.1016/j.cell.2009.08.034)
44. Aso Y et al. 2012 Three dopamine pathways induce aversive odor memories with different stability. PLoS Genet. 8, e1002768. (doi:10.1371/journal.pgen.1002768)
45. Nogi Y, Shimada H, Matsuzaki Y, Hashimoto H, Fukasawa T. 1984 Regulation of expression of the galactose gene cluster in Saccharomyces cerevisiae. II. The isolation and dosage effect of the regulatory gene GAL80. Mol. Gen. Genet. 195, 29–34. (doi:10.1007/BF00332719)
46. Lee T, Luo L. 1999 Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451–461. (doi:10.1016/S0896-6273(00)80701-1)
47. Kitamoto T. 2002 Conditional disruption of synaptic transmission induces male-male courtship behavior in Drosophila. Proc. Natl Acad. Sci. USA 99, 13 232–13 237. (doi:10.1073/pnas.202489099)
48. Sitaraman D, Zars M, Laferriere H, Chen Y-C, Sable- Smith A, Kitamoto T, Rottinghaus GE, Zars T. 2008 Serotonin is necessary for place memory in Drosophila. Proc. Natl Acad. Sci. USA 105, 5579–5584. (doi:10.1073/pnas.0710168105)
49. Bussell JJ, Yapici N, Zhang SX, Dickson BJ, Vosshall LB. 2014 Abdominal-B neurons control Drosophila virgin female receptivity. Curr. Biol. 24, 1584–1595. (doi:10.1016/j.cub.2014.06.011)
50. Clyne JD, Miesenbock G. 2008 Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133, 354–363. (doi:10.1016/j.cell.2008.01.050)
51. Waddell S, Quinn WG. 2001 Flies, genes, and learning. Annu. Rev. Neurosci. 24, 1283–1309. (doi:10.1146/annurev.neuro.24.1.1283)
52. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003 Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765–1768. (doi:10.1126/science.1089035)
53. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M. 2001 Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523–1531.
54. White BH, Osterwalder TP, Yoon KS, Joiner WJ, Whim MD, Kaczmarek LK, Keshishian H. 2001 Targeted attenuation of electrical activity in Drosophila using a genetically modified Kþ channel. Neuron 31, 699–711. (doi:10.1016/S0896-6273(01)00415-9)
55. Nitabach MN, Blau J, Holmes TC. 2002 Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109, 485–495. (doi:10.1016/S0092-8674(02)00737-7)
56. Sweeney ST, Broadie K, Keane J, Niemann H, O’Kane CJ. 1995 Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341–351. (doi:10.1016/0896-6273(95)90290-2)
57. Ferris J, Ge H, Liu L, Roman G. 2006 G(o) signaling is required for Drosophila associative learning. Nat. Neurosci. 9, 1036–1040. (doi:10.1038/nn1738)
58. Clemens JC, Worby CA, Simonson-Leff N, Muda M, Maehama T, Hemmings BA, Dixon JE. 2000 Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl Acad. Sci. USA 97, 6499–6503. (doi:10.1073/pnas.110149597)
59. Dietzl G et al. 2007 A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151–156. (doi:10.1038/nature05954)
60. Potter CJ, Tasic B, Russler EV, Liang L, Luo L. 2010 The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141, 536–548. (doi:10.1016/j.cell.2010.02.025)
61. Shang Y, Griffith LC, Rosbash M. 2008 Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc. Natl Acad. Sci. USA 105, 19 587–19 594. (doi:10.1073/pnas.0809577105)
62. Perrat PN, DasGupta S, Wang J, Theurkauf W, Weng Z, Rosbash M, Waddell S. 2013 Transposition-driven genomic heterogeneity in the Drosophila brain. Science 340, 91–95. (doi:10.1126/science.1231965)
63. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ. 2005 Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795–807. (doi:10.1016/j.cell.2005.04.026)
64. Luan H, Peabody NC, Vinson CR, White BH. 2006 Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52, 425–436. (doi:10.1016/j.neuron.2006.08.028)
65. Aso Y et al. 2014 The neuronal architecture of the mushroom body provides a logic for associative learning. Elife 3, e04577. (doi:10.7554/eLife.04577)
66. Ting CY, Gu S, Guttikonda S, Lin TY, White BH, Lee CH. 2011 Focusing transgene expression in Drosophila by coupling Gal4 with a novel split-LexA expression system. Genetics 188, 229–233. (doi:10.1534/genetics.110.126193)
67. Gohl DM et al. 2011 A versatile in vivo system for directed dissection of gene expression patterns. Nat. Methods 8, 231–237. (doi:10.1038/nmeth.1561)
68. Diao F et al. 2015 Plug-and-play genetic access to Drosophila cell types using exchangeable exon cassettes. Cell Rep. 10, 1410–1421. (doi:10.1016/j.celrep.2015.01.059)
69. Poodry CA, Hall L, Suzuki DT. 1973 Developmental properties of shibirets1: a pleiotropic mutation affecting larval and adult locomotion and development. Dev. Biol. 32, 373–386. (doi:10.1016/0012-1606(73)90248-0)
70. Kelly LE, Suzuki DT. 1974 The effects of increased temperature on electroretinograms of temperaturesensitive paralysis mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 71, 4906–4909. (doi:10.1073/pnas.71.12.4906)
71. Ikeda K, Ozawa S, Hagiwara S. 1976 Synaptic transmission reversibly conditioned by single-gene mutation in Drosophila melanogaster. Nature 259, 489–491. (doi:10.1038/259489a0)
72. Koenig JH, Saito K, Ikeda K. 1983 Reversible control of synaptic transmission in a single gene mutant of Drosophila melanogaster. J. Cell Biol. 96, 1517–1522. (doi:10.1083/jcb.96.6.1517)
73. Kosaka T, Ikeda K. 1983 Reversible blockage of membrane retrieval and endocytosis in the garland cell of the temperature-sensitive mutant of Drosophila melanogaster, shibirets1. J. Cell Biol. 97, 499–507. (doi:10.1083/jcb.97.2.499)
74. van der Bliek AM, Meyerowitz EM. 1991 Dynaminlike protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411–414. (doi:10.1038/351411a0)
75. Chen MS, Obar RA, Schroeder CC, Austin TW, Poodry CA, Wadsworth SC, Vallee RB. 1991 Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351, 583–586. (doi:10.1038/351583a0)
76. Kawasaki F, Hazen M, Ordway RW. 2000 Fast synaptic fatigue in shibire mutants reveals a rapid requirement for dynamin in synaptic vesicle membrane trafficking. Nat. Neurosci. 3, 859–860. (doi:10.1038/78753)
77. Kitamoto T. 2001 Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47, 81–92. (doi:10.1002/neu.1018)
78. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG. 2000 The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103, 805–813. (doi:10.1016/S0092-8674(00)00183-5)
79. Dubnau J, Grady L, Kitamoto T, Tully T. 2001 Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411, 476–480. (doi:10.1038/35078077)
80. McGuire SE, Le PT, Davis RL. 2001 The role of Drosophila mushroom body signaling in olfactory memory. Science 293, 1330–1333. (doi:10.1126/science.1062622)
81. Keene AC, Krashes MJ, Leung B, Bernard JA, Waddell S. 2006 Drosophila dorsal paired medial neurons provide a general mechanism for memory consolidation. Curr. Biol. 16, 1524–1530. (doi:10.1016/j.cub.2006.06.022)
82. Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S. 2007 Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53, 103–115. (doi:10.1016/j.neuron.2006.11.021)
83. Krashes MJ, Waddell S. 2008 Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. J. Neurosci. 28, 3103–3113. (doi:10.1523/JNEUROSCI.5333-07.2008)
84. Trannoy S, Redt-Clouet C, Dura JM, Preat T. 2011 Parallel processing of appetitive short- and longterm memories in Drosophila. Curr. Biol. 21, 1647–1653. (doi:10.1016/j.cub.2011.08.032)
85. Cervantes-Sandoval I, Martin-Pena A, Berry JA, Davis RL. 2013 System-like consolidation of olfactory memories in Drosophila. J. Neurosci. 33, 9846–9854. (doi:10.1523/JNEUROSCI.0451-13.2013)
86. Johard HA, Enell LE, Gustafsson E, Trifilieff P, Veenstra JA, Nassel DR. 2008 Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. J. Comp. Neurol. 507, 1479–1496. (doi:10.1002/cne.21636)
87. Zemelman BV, Lee GA, Ng M, Miesenbock G. 2002 Selective photostimulation of genetically chARGed neurons. Neuron 33, 15–22. (doi:10.1016/S0896-6273(01)00574-8)
88. Lima SQ, Miesenbock G. 2005 Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141–152. (doi:10.1016/j.cell.2005.02.004)
89. Nagel G et al. 2003 Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl Acad. Sci. USA 100, 13 940–13 945. (doi:10.1073/pnas.1936192100)
90. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005 Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263–1268. (doi:10.1038/nn1525)
91. Schroll C et al. 2006 Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16, 1741–1747. (doi:10.1016/j.cub.2006.07.023)
92. Suh GS, Ben-Tabou de Leon S, Tanimoto H, Fiala A, Benzer S, Anderson DJ. 2007 Light activation of an innate olfactory avoidance response in Drosophila. Curr. Biol. 17, 905–908. (doi:10.1016/j.cub.2007.04.046)
93. Gordon MD, Scott K. 2009 Motor control in a Drosophila taste circuit. Neuron 61, 373–384. (doi:10.1016/j.neuron.2008.12.033)
94. Root CM, Masuyama K, Green DS, Enell LE, Na¨ssel DR, Lee C-H, Wang JW. 2008 A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59, 311–321. (doi:10.1016/j.neuron.2008.07.003)
95. Gruntman E, Turner GC. 2013 Integration of the olfactory code across dendritic claws of single mushroom body neurons. Nat. Neurosci. 16, 1821–1829. (doi:10.1038/nn.3547)
96. Gaudry Q, Hong EJ, Kain J, de Bivort BL, Wilson RI. 2013 Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila. Nature 493, 424–428. (doi:10.1038/nature11747)
97. Yaksi E, Wilson RI. 2010 Electrical coupling between olfactory glomeruli. Neuron 67, 1034–1047. (doi:10.1016/j.neuron.2010.08.041)
98. Nagel KI, Hong EJ, Wilson RI. 2015 Synaptic and circuit mechanisms promoting broadband transmission of olfactory stimulus dynamics. Nat. Neurosci. 18, 56–65. (doi:10.1038/nn.3895)
99. Lin JY, Knutsen PM, Muller A, Kleinfeld D, Tsien RY. 2013 ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat. Neurosci. 16, 1499–1508. (doi:10.1038/nn.3502)
100. Inagaki HK, Jung Y, Hoopfer ED, Wong AM, Mishra N, Lin JY, Tsien RY, Anderson DJ. 2014 Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat. Methods 11, 325–332. (doi:10.1038/nmeth.2765)
101. Owald D, Felsenberg J, Talbot CB, Das G, Perisse E, Huetteroth W, Waddell S. 2015 Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila. Neuron 86, 417–427. (doi:10.1016/j.neuron.2015.03.025)
102. Klapoetke NC et al. 2014 Independent optical excitation of distinct neural populations. Nat. Methods 11, 338–346. (doi:10.1038/nmeth.2836)
103. Aso Y et al. 2014 Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. Elife 4, e04580. (doi:10.7554/eLife.04580)
104. Dawydow A et al. 2014 Channelrhodopsin-2-XXL, a powerful optogenetic tool for low-light applications. Proc. Natl Acad. Sci. USA 111, 13 972–13 977. (doi:10.1073/pnas.1408269111)
105. AzimiHashemi N et al. 2014 Synthetic retinal analogues modify the spectral and kinetic characteristics of microbial rhodopsin optogenetic tools. Nat. Commun. 5, 5810. (doi:10.1038/ncomms6810)
106. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA. 2008 An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217–220. (doi:10.1038/nature07001)
107. McKemy DD, Neuhausser WM, Julius D. 2002 Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416, 52–58. (doi:10.1038/nature719)
108. Peier AM et al. 2002 A TRP channel that senses cold stimuli and menthol. Cell 108, 705–715. (doi:10.1016/S0092-8674(02)00652-9)
109. Parisky KM et al. 2008 PDF cells are a GABAresponsive wake-promoting component of the Drosophila sleep circuit. Neuron 60, 672–682. (doi:10.1016/j.neuron.2008.10.042)
110. Donlea JM, Thimgan MS, Suzuki Y, Gottschalk L, Shaw PJ. 2011 Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 332, 1571–1576. (doi:10.1126/science.1202249)
111. Schwaerzel M, Monastirioti M, Scholz H, Friggi- Grelin F, Birman S, Heisenberg M. 2003 Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23, 10 495–10 502.
112. Aso Y, Siwanowicz I, Bracker L, Ito K, Kitamoto T, Tanimoto H. 2010 Specific dopaminergic neurons for the formation of labile aversive memory. Curr. Biol. 20, 1445–1451. (doi:10.1016/j.cub.2010.06.048)
113. Yamagata N, Ichinose T, Aso Y, Plaçais P-Y, Friedrich AB, Sima RJ, Preat T, Rubin GM, Tanimoto H. 2015 Distinct dopamine neurons mediate reward signals for short- and long-term memories. Proc. Natl Acad. Sci. USA 112, 578–583. (doi:10.1073/pnas.1421930112)
114. Huetteroth W, Perisse E, Lin S, Klappenbach M, Burke C, Waddell S. 2015 Sweet taste and nutrient value subdivide rewarding dopaminergic neurons in Drosophila. Curr. Biol. 25, 751–758. (doi:10.1016/j.cub.2015.01.036)
115. Zemelman BV, Nesnas N, Lee GA, Miesenbock G. 2003 Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc. Natl Acad. Sci. USA 100, 1352–1357. (doi:10.1073/pnas.242738899)
116. Peabody NC, Pohl JB, Diao F, Vreede AP, Sandstrom DJ, Wang H, Zelensky PK, White BH. 2009 Characterization of the decision network for wing expansion in Drosophila using targeted expression of the TRPM8 channel. J. Neurosci. 29, 3343–3353. (doi:10.1523/JNEUROSCI.4241-08.2009)
117. Flood TF, Gorczyca M, White BH, Ito K, Yoshihara M. 2013 A large-scale behavioral screen to identify neurons controlling motor programs in the Drosophila brain. G3 (Bethesda) 3, 1629–1637. (doi:10.1534/g3.113.006205)
118. Flood TF, Iguchi S, Gorczyca M, White B, Ito K, Yoshihara M. 2013 A single pair of interneurons commands the Drosophila feeding motor program. Nature 499, 83–87. (doi:10.1038/nature12208)
119. Bidaye SS, Machacek C, Wu Y, Dickson BJ. 2014 Neuronal control of Drosophila walking direction. Science 344, 97–101. (doi:10.1126/science.1249964)
120. Seeds AM, Ravbar P, Chung P, Hampel S, Midgley FM, Mensh BD, Simpson JH. 2014 A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila. Elife 3, e02951. (doi:10.7554/eLife.02951)
121. Hergarden AC, Tayler TD, Anderson DJ. 2012 Allatostatin-A neurons inhibit feeding behavior in adult Drosophila. Proc. Natl Acad. Sci. USA 109, 3967–3972. (doi:10.1073/pnas.1200778109)
122. Kohatsu S, Koganezawa M, Yamamoto D. 2011 Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69, 498–508. (doi:10.1016/j.neuron.2010.12.017)
123. Tayler TD, Pacheco DA, Hergarden AC, Murthy M, Anderson DJ. 2012 A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila. Proc. Natl Acad. Sci. USA 109, 20 697–20 702. (doi:10.1073/pnas.1218246109)
124. Asahina K, Watanabe K, Duistermars BJ, Hoopfer E, González CR, Eyjólfsdóttir EA, Perona P, Anderson DJ. 2014 Tachykinin-expressing neurons control malespecific aggressive arousal in Drosophila. Cell 156, 221–235. (doi:10.1016/j.cell.2013.11.045)
125. Vasmer D, Pooryasin A, Riemensperger T, Fiala A. 2014 Induction of aversive learning through thermogenetic activation of Kenyon cell ensembles in Drosophila. Front. Behav. Neurosci. 8, 174. (doi:10.3389/fnbeh.2014.00174)
126. Herman AM, Huang L, Murphey DK, Garcia I, Arenkiel BR. 2014 Cell type-specific and timedependent light exposure contribute to silencing in neurons expressing Channelrhodopsin-2. Elife 3, e01481. (doi:10.7554/eLife.01481)
127. Miyawaki A, Griesbeck O, Heim R, Tsien RY. 1999 Dynamic and quantitative Ca2þ measurements using improved cameleons. Proc. Natl Acad. Sci. USA 96, 2135–2140. (doi:10.1073/pnas.96.5.2135)
128. Kerr R, Lev-Ram V, Baird G, Vincent P, Tsien RY, Schafer WR. 2000 Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26, 583–594. (doi:10.1016/S0896-6273(00)81196-4)
129. Nakai J, Ohkura M, Imoto K. 2001 A high signal-tonoise Ca2þ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19, 137–141. (doi:10.1038/84397)
130. Tian L et al. 2009 Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods. 6, 875–881. (doi:10.1038/nmeth.1398)
131. Zhao Y et al. 2011 An expanded palette of genetically encoded Ca2þ indicators. Science 333, 1888–1891. (doi:10.1126/science.1208592)
132. Akerboom J et al. 2013 Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 6, 2. (doi:10.3389/fnmol.2013.00002)
133. Chen TW et al. 2013 Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300. (doi:10.1038/nature12354)
134. Miesenbock G, De Angelis DA, Rothman JE. 1998 Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192–195. (doi:10.1038/28190)
135. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ. 2004 Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279, 37 215–37 218. (doi:10.1074/jbc.C400302200)
136. Jin L, Han Z, Platisa J, Wooltorton JR, Cohen LB, Pieribone VA. 2012 Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 75, 779–785. (doi:10.1016/j.neuron.2012.06.040)
137. Gong Y, Wagner MJ, Zhong Li J, Schnitzer MJ. 2014 Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat. Commun. 5, 3674. (doi:10.1038/ncomms4674)
138. Rosay P, Armstrong JD, Wang Z, Kaiser K. 2001 Synchronized neural activity in the Drosophila memory centers and its modulation by amnesiac. Neuron 30, 759–770. doi:10.1016/S0896-6273(01)00323-3
139. Fiala A, Spall T, Diegelmann S, Eisermann B, Sachse S, Devaud J-M, Buchner E, Galizia CG. 2002 Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr. Biol. 12, 1877–1884. (doi:10.1016/S0960-9822(02)01239-3)
140. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenbock G. 2002 Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463–474. (doi:10.1016/S0896-6273(02)00975-3)
141. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R. 2003 Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271–282. (doi:10.1016/S0092-8674(03)432#00004-7)
142. Yu D, Akalal DB, Davis RL. 2006 Drosophila alpha/ beta mushroom body neurons form a branchspecific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52, 845–855. (doi:10.1016/j.neuron.2006.10.030)
143. Wang Y, Mamiya A, Chiang AS, Zhong Y. 2008 Imaging of an early memory trace in the Drosophila mushroom body. J. Neurosci. 28, 4368–4376. (doi:10.1523/JNEUROSCI.2958-07.2008)
144. Akalal DB, Yu D, Davis RL. 2010 A late-phase, longterm memory trace forms in the gamma neurons of Drosophila mushroom bodies after olfactory classical conditioning. J. Neurosci. 30, 16 699–16 708. (doi:10.1523/JNEUROSCI.1882-10.2010)
145. Zhang S, Roman G. 2013 Presynaptic inhibition of gamma lobe neurons is required for olfactory learning in Drosophila. Curr. Biol. 23, 2519–2527. (doi:10.1016/j.cub.2013.10.043)
146. Yu D, Keene AC, Srivatsan A, Waddell S, Davis RL. 2005 Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 123, 945–957. (doi:10.1016/j.cell.2005.09.037)
147. Cervantes-Sandoval I, Davis RL. 2012 Distinct traces for appetitive versus aversive olfactory memories in DPM neurons of Drosophila. Curr. Biol. 22, 1247–1252. (doi:10.1016/j.cub.2012.05.009)
148. Liu X, Davis RL. 2009 The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning. Nat. Neurosci. 12, 53–59. (doi:10.1038/nn.2235)
149. Akalal DB, Yu D, Davis RL. 2011 The long-term memory trace formed in the Drosophila alpha/beta mushroom body neurons is abolished in long-term memory mutants. J. Neurosci. 31, 5643–5647. (doi:10.1523/JNEUROSCI.3190-10.2011)
150. Wang Y et al. 2004 Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2þ imaging. J. Neurosci. 24, 6507–6514. (doi:10.1523/JNEUROSCI.3727-03.2004)
151. Honegger KS, Campbell RA, Turner GC. 2011 Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J. Neurosci. 31, 11 772–11 785. (doi:10.1523/JNEUROSCI.1099-11.2011)
152. Lin AC, Bygrave AM, de Calignon A, Lee T, Miesenbock G. 2014 Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination. Nat. Neurosci. 17, 559–568. (doi:10.1038/nn.3660)
153. Riemensperger T, Voller T, Stock P, Buchner E, Fiala A. 2005 Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 15, 1953–1960. (doi:10.1016/j.cub.2005.09.042)
154. Mao Z, Davis RL. 2009 Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front. Neural Circuits 3, 5. (doi:10.3389/neuro.04.005.2009)
155. Placais PY et al. 2012 Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila. Nat. Neurosci. 15, 592–599. (doi:10.1038/nn.3055)
156. Berry JA, Cervantes-Sandoval I, Nicholas EP, Davis RL. 2012 Dopamine is required for learning and forgetting in Drosophila. Neuron 74, 530–542. (doi:10.1016/j.neuron.2012.04.007)
157. Sejourne J et al. 2011 Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat. Neurosci. 14, 903–910. (doi:10.1038/nn.2846)
158. Placais PY, Trannoy S, Friedrich AB, Tanimoto H, Preat T. 2013 Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in Drosophila. Cell Rep. 5, 769–780. (doi:10.1016/j.celrep.2013.09.032)
159. Pai TP, Chen CC, Lin HH, Chin A-L, Lai JS-Y, Lee P-T, Tully T, Chiang A-S. 2013 Drosophila ORB protein in two mushroom body output neurons is necessary for longterm memory formation. Proc. Natl Acad. Sci. USA 110, 7898–7903. (doi:10.1073/pnas.1216336110)
160. Cao G, Platisa J, Pieribone VA, Raccuglia D, Kunst M, Nitabach MN. 2013 Genetically targeted optical electrophysiology in intact neural circuits. Cell 154, 904–913. (doi:10.1016/j.cell.2013.07.027)
161. Shafer OT, Kim DJ, Dunbar-Yaffe R, Nikolaev VO, Lohse MJ, Taghert PH. 2008 Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58, 223–237. (doi:10.1016/j.neuron.2008.02.018)
162. Yao Z, Shafer OT. 2014 The Drosophila circadian clock is a variably coupled network of multiple peptidergic units. Science 343, 1516–1520. (doi:10.1126/science.1251285)
163. Zhang J, Hupfeld CJ, Taylor SS, Olefsky JM, Tsien RY. 2005 Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes. Nature 437, 569–573. (doi:10.1038/nature04140)
164. Tomchik SM, Davis RL. 2009 Dynamics of learningrelated cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64, 510–521. (doi:10.1016/j.neuron.2009.09.029)
165. Gervasi N, Tchenio P, Preat T. 2010 PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron 65, 516–529. (doi:10.1016/j.neuron.2010.01.014)
166. Inagaki HK et al. 2012 Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugar sensing. Cell 148, 583–595. (doi:10.1016/j.cell.2011.12.022)
167. Boto T, Louis T, Jindachomthong K, Jalink K, Tomchik SM. 2014 Dopaminergic modulation of cAMP drives nonlinear plasticity across the Drosophila mushroom body lobes. Curr. Biol. 24, 822–831. (doi:10.1016/j.cub.2014.03.021)
168. Klarenbeek JB, Goedhart J, Hink MA, Gadella TW, Jalink K. 2011 A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS ONE 6, e19170. (doi:10.1371/journal.pone.0019170)
169. Allen MD, Zhang J. 2006 Subcellular dynamics of protein kinase A activity visualized by FRET-based reporters. Biochem. Biophys. Res. Commun. 348, 716–721. (doi:10.1016/j.bbrc.2006.07.136)
170. Hu A, Zhang W, Wang Z. 2010 Functional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway. Proc. Natl Acad. Sci. USA 107, 10 262–10 267. (doi:10.1073/pnas.0914912107)
171. Liu WW, Wilson RI. 2013 Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system. Proc. Natl Acad. Sci. USA 110, 10 294–10 299. (doi:10.1073/pnas.1220560110)
172. Mauss AS, Meier M, Serbe E, Borst A. 2014 Optogenetic and pharmacologic dissection of feedforward inhibition in Drosophila motion vision. J. Neurosci. 34, 2254–2263. (doi:10.1523/JNEUROSCI.3938-13.2014)
173. Peled ES, Newman ZL, Isacoff EY. 2014 Evoked and spontaneous transmission favored by distinct sets of synapses. Curr. Biol. 24, 484–493. (doi:10.1016/j.cub.2014.01.022)
174. Melom JE, Akbergenova Y, Gavornik JP, Littleton JT. 2013 Spontaneous and evoked release are independently regulated at individual active zones. J. Neurosci. 33, 17 253–17 263. (doi:10.1523/JNEUROSCI.3334-13.2013)
175. Ljaschenko D, Ehmann N, Kittel RJ. 2013 Hebbian plasticity guides maturation of glutamate receptor fields in vivo. Cell Rep. 3, 1407–1413. (doi:10.1016/j.celrep.2013.04.003)
176. Kauwe G, Isacoff EY. 2013 Rapid feedback regulation of synaptic efficacy during high-frequency activity at the Drosophila larval neuromuscular junction. Proc. Natl Acad. Sci. USA 110, 9142–9147. (doi:10.1073/pnas.1221314110)
177. Maimon G, Straw AD, Dickinson MH. 2010 Active flight increases the gain of visual motion processing in Drosophila. Nat. Neurosci. 13, 393–399. (doi:10.1038/nn.2492)
178. Seelig JD, Chiappe ME, Lott GK, Dutta A, Osborne JE, Reiser MB, Jayaraman V. 2010 Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nat. Methods 7, 535–540. (doi:10.1038/nmeth.1468)